IMPLEMENTATION
AND
OPERATIONAL RESEARCH: EPIDEMIOLOGY
AND
PREVENTION
Linkage to HIV Care and Antiretroviral Therapy by HIV
Testing Service Type in Central Mozambique: A
Retrospective Cohort Study
Sarah E. Gerdts, MPH,* Bradley H. Wagenaar, MPH,*† Mark A. Micek, MD, MPH,†‡
Carey Farquhar, MD, MPH,*‡ Marina Kariaganis, MD,§ Juvenal Amos, MD, MPH,§
Sarah Gimbel, RN, PhD, MPH,‡k James Pfeiffer, PhD, MPH,†‡ Stephen Gloyd, MD, MPH,†‡
and Kenneth Sherr, PhD, MPH†‡
Background: Access to antiretroviral therapy (ART) has increased
dramatically in resource-limited settings since its introduction
a decade ago. However, ART coverage remains low in countries
with the highest disease burden, which may be partially explained by
poor testing to care linkages. HIV testing service may impact early
attrition in the HIV treatment cascade.
Methods: A retrospective cohort study was conducted in 18 clinics
in central Mozambique using routine patient data and monthly
reports. Patients referred from voluntary counseling and testing
(VCT) were compared with those referred from prevention of
mother-to-child transmission (PMTCT) for 3 outcomes: (1) enrollment at an HIV clinic #30 days after testing HIV positive, (2) CD4
test #30 days after enrollment, and (3) ART initiation #90 days
after first CD4 test.
Results: Patient retention in the HIV care system dropped at each
step from HIV testing to ART initiation. Enrollment in HIV care was
not significantly different between PMTCT and VCT [risk ratio
(RR) = 0.84, 0.72 , RR , 1.02]. Women tested in PMTCT were
less likely to have a CD4 test #30 days after enrollment when
adjusting for age, education level, and marital status (adjusted
RR = 0.84, 0.70 , RR , 1.00), and were less likely to initiate
Received for publication November 22, 2013; accepted November 22, 2013.
From the *Department of Epidemiology, University of Washington, Seattle,
WA; †Health Alliance International, Seattle, WA; ‡Department of Global
Health, University of Washington, Seattle, WA; §Ministry of Health,
Mozambique; and kDepartment of Family Child Nursing, University of
Washington, Seattle, WA (Micek is now with the Department of Medicine,
University of Wisconsin–Madison, Madison, WI, USA).
The authors have no funding or conflicts of interest to disclose.
Supported by the President’s Emergency Plan for AIDS Relief, the African
Health Initiative of the Doris Duke Charitable Foundation, and NIAID,
NCI, NIMH, NIDA, NICHD, NHLBI, NIA, NIGMS, NIDDK of the
National Institutes of Health under award number P30AI027757. K. S.
was supported by Grant Number K02TW009207 from the Fogarty International Center. The content is solely the responsibility of the authors and
does not necessarily represent the official views of the National Institutes
of Health.
Supplemental digital content is available for this article. Direct URL citations
appear in the printed text and are provided in the HTML and PDF
versions of this article on the journal’s Web site (www.jaids.com).
Correspondence to: Kenneth Sherr, PhD, MPH, University of Washington,
107 45th Avenue NE, Seattle, WA 98105 (e-mail: [email protected]).
Copyright © 2013 by Lippincott Williams & Wilkins
ART #90 days after their first CD4 test when adjusting for age,
education, and marital status (adjusted RR = 0.56, 0.44 , RR , 0.71).
Conclusions: Poor linkages between HIV testing and care hamper
efforts to improve coverage for HIV care and treatment services.
Increased loss to follow-up among women diagnosed in PMTCT
relative to VCT is worrisome and merits further qualitative research
and programmatic attention.
Key Words: linkages, HIV testing, antiretroviral therapy, Mozambique, HIV testing to care, operations research
(J Acquir Immune Defic Syndr 2014;66:e37–e44)
INTRODUCTION
Mozambique ranks among the top 10 countries with the
highest adult HIV prevalence globally.1 HIV prevalence patterns vary regionally in Mozambique, and in the central provinces of Manica and Sofala, adult HIV prevalence is
estimated to be 15.3% and 15.5%, respectively.2 In response
to the HIV epidemic, Mozambique rapidly expanded antiretroviral therapy (ART) coverage through a national HIV care
plan launched in 2004, and the proportion of eligible adults
on ART grew from less than 3% in 2003 to 51.7% in 2011.3
Although this increase in ART coverage is impressive, over
a quarter of a million HIV-infected ART-eligible adults are
still not accessing ART.3
The success of an ART program depends on its ability
to find, enroll, treat, and maintain access to care for HIVpositive patients. Loss to follow-up (LTFU) is high at each
step in the HIV treatment cascade, varies greatly between
treatment clinics, and is especially high before patients begin
ART.4–6 LTFU is a complex issue that can be influenced by
multiple factors on the individual, health care system, and
societal levels.7–11 Assessing follow-up across the treatment
cascade is important in LTFU studies because it identifies
bottlenecks that can be targeted to achieve improvements in
ART coverage.5
One characteristic associated with LTFU is the type of
HIV testing center. Studies conducted previously in Mozambique suggest that pregnant women who were identified as
HIV infected at prevention of mother-to-child transmission
(PMTCT) centers are less likely to be linked to HIV care and
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Gerdts et al
initiate ART compared with people identified at voluntary
counseling and testing (VCT) centers.5 A number of factors
could contribute to this difference in retention among testing
service types. First, self-referral has been associated with
lower LTFU compared with provider-initiated HIV testing,
and PMTCT testing is generally provider initiated.12 Second,
PMTCT attendees are often healthier, with higher CD4
counts, which has also been associated with higher LTFU.11,13
Additionally, HIV-positive pregnant women may be particularly vulnerable to the burdens of an HIV diagnosis, including
concern for the fetus, stigma, uncertainty about disclosure,
and additional health care visits necessary for antenatal care.14
To better understand the impact of HIV testing
approach on patient flow through HIV care systems, we
retrospectively examined a cohort of patients who were
identified as HIV infected at VCT and PMTCT and were
followed-up through ART initiation at 18 public sector clinics
with ART services in central Mozambique.
Patients were excluded from analyses if they were
known to have transferred to another clinic or died within the
follow-up period for a given outcome, or if their enrollment
date was earlier than their test date, their CD4 test date was
earlier than their enrollment date, or if their ART start date
was earlier than their first CD4 test date.
Data Sources
This study used routine data from HIV testing centers
and ART clinics. HIV testing service data provided the
number of patients receiving an HIV diagnosis per month via
routine facility monthly reports. ART clinic data included site
and date of HIV testing, sociodemographic information
collected at the time of enrollment, and clinical, laboratory,
and pharmacy information collected at each patient visit to the
clinic. Facility-based personnel maintained the databases
primarily for routine program monitoring purposes, and the
clinic databases have been validated over the study
period.5,15–18
METHODS
Study Setting
Variable Definition and Covariates
This study included patients identified as HIV infected
at PMTCT and VCT centers within the HIV care networks of
18 public-sector ART clinics in the central Mozambique
provinces of Manica and Sofala. The first 4 ART clinics in the
region began between 2003 and 2005 as centralized centers
that received patients from satellite HIV testing locations.15,16
As the HIV care network expanded, PMTCT centers were
integrated into antenatal care, VCT centers were integrated
into HIV care facilities, and ART clinics were integrated into
primary health care.16 During the study period, 15 of the 18
ART clinics had an integrated delivery model, 10 were urban,
and 6 were hospitals. Although HIV testing and care centers
became widely available throughout Manica and Sofala provinces during the study period, only 18 ART clinics and associated HIV testing services were included in this study as they
had patient-level electronic data systems.
Detailed definitions used for linkage outcomes and
exclusions are presented in Table 1. For analyses of ART
treatment outcomes, LTFU was defined as a patient not
returning to pick up their medication for .60 days. Patientlevel covariates were considered for inclusion in analysis
Study Population
Study subjects were patients who tested HIV positive
between January 1, 2007, and May 1, 2008, at a PMTCT or
VCT center in the direct catchment area of the 18 included
ART clinics. Analysis was restricted to ART naive adults (age
$ 15 years) who newly enrolled in HIV care at the ART
clinics. Study subjects were assessed for 3 outcomes: (1)
enrollment at an ART clinic #30 days after testing HIV
positive, (2) completion of a CD4 test #30 days after ART
clinic enrollment, and (3) initiation of ART (if eligible) #90
days after the first CD4 test.
Irrespective of the testing site, newly identified HIVpositive patients were referred to an ART care facility and
told to present their HIV test card upon arrival. This HIV test
card contained information on HIV test date, location, and
results of HIV testing. After enrollment at an ART clinic,
patients were told to return within #2 weeks for the results of
their CD4 test.
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TABLE 1. Variable Definitions and Exclusions for HIV Testing
Center Type and 3 HIV Linkage Outcomes
Factor
HIV testing
center
type
Outcome 1:
ART
clinic
enrollment
Outcome 2:
CD4
testing
Outcome 3:
ART
initiation
Definition
Determined by name of
testing center in patient’s
ART file compiled from
paper referral forms given
to patients at HIV
diagnosis
Patients “successfully
enrolled” at ART clinic if
#30 d from testing HIV
positive
Exclusions
Any males tested at
PMTCT centers
If listed HIV testing center
and HIV test date
corresponded with
missing monthly total of
HIV-positive tests at the
given center
Those undergoing CD4 test
#30 d after “successful”
ART enrollment
ART initiation #90 d after
“successful” CD4 testing
for all ART-eligible
patients. ART eligibility
based on national
guidelines defined as
patients with CD4 ,200
cells per mm3, patients
with CD4 counts ,350
cells per mm3 who were
also in WHO clinical
stage 3 or pregnant, and
all patients in WHO
clinical stage 4 regardless
of CD4 count
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based on their theoretical potential to confound the relationship between HIV testing location and study outcomes.
Statistical Analysis
Outcome percentages were calculated by dividing the
numerator (the number of patients who went on to the next
step in the treatment cascade within the allotted time frame)
by the denominator (the number of patients from the previous
step minus the patients who were excluded for the outcome
being calculated). Cumulative percentages were based on the
original number of patients who tested HIV positive and were
calculated by multiplying the percentages that moved on at
each step in the treatment cascade.
Generalized linear models for the binomial family were
used to estimate the association between site of HIV testing and
each of the study outcomes. Risk ratios (RR) were estimated
using the log link function. Analyses of CD4 and ART
outcomes accounted for clinic-level clustering using generalized
Linkages From HIV Testing to Care
estimating equations, and analysis of enrollment was clustered
at the level of HIV testing service. Analyses of ART treatment
outcomes used the standard life table approach and competing
risks cause-specific cumulative incidence calculations.
The study was approved by the institutional review
boards of the Mozambique Ministry of Health and the
University of Washington. All analyses were conducted in
Stata 13 (College Station, TX).
RESULTS
Cohort Characteristics
In the ART clinic databases, 24,820 (74%) of 33,640
patients who tested HIV positive were matched to the testing
center data by the month and site of HIV testing (Fig. 1).
Of these, 2083 (8.4%) patients did not meet the eligibility
criteria due to the following: age ,15 years (n = 1628), not
the first ART clinic enrollment (n = 263), male tested at PMTCT
FIGURE 1. Study flow chart stratified by HIV care type (VCT vs. PMTCT). Patients were dropped if younger than 15 years (N =
1628), missing age (N = 30), not HIV positive (N = 16), not the first ART clinic enrollment (N = 263, 1.1%), male tested at PMTCT
(N = 113), or enrolled before 2007 (N = 33). Patients were excluded from analysis of outcome 1 because their enrollment date
was earlier than their HIV test date. Patients were excluded from analysis of outcome 2 because 341 (1.6%) left the clinic within 30
days of enrollment due to transfer or death, 325 (1.5%) had a CD4 test date listed as earlier than their enrollment date, and 1
(,0.0%) had a CD4 test but did not have a listed CD4 date. Patients were excluded from the ART analysis because 434 (6.3%)
died or transferred clinics #90 days after their first CD4 test and 12 (0.2%) had an ART start date that was earlier than their first
CD4 date.
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(n = 113), enrollment before 2007 (n = 33), missing age (n = 30),
or not HIV infected (n = 16). Thus, a total of 22,737 patients
enrolling in an ART clinic were included in this study.
Of these 22,737 patients, 151 (0.7%) were excluded
from the enrollment analysis because their recorded enrollment date was before their HIV test date. A total of 667
(2.9%) were excluded from the CD4 analysis due to transfer
or death within 30 days of enrollment (n = 341, 1.6%), having
a CD4 test date was earlier than their enrollment date (n =
325, 1.5%), or having a CD4 test without a listed CD4 date
(1, ,0.0%). A total of 446 patients (6.5%) were excluded
from the ART analysis due to death or clinic transfer #90
days after their first CD4 test (434, 6.3%) or an ART start date
that preceded the first CD4 date (12, 0.2%). The proportion of
patients who were known to be lost due to death or transfer
within 120 days of clinic enrollment was greater in VCT (n =
937, 5.6%) than PMTCT (n = 34, 0.6%).
Demographic characteristics of the 22,737 patients
enrolled in ART clinics are presented in Table 2. Briefly, those
tested at VCT centers were on average almost 10 years older, had
higher education levels, were less likely to be married, had lower
baseline CD4 counts, were more likely to be in WHO stage III or
IV, and were more likely to attend a vertical ART clinic.
positive [22,582 (99%) enrolled at some point]. A total of
13,708 (63%) completed a CD4 test #30 days of enrollment
at an ART clinic [14,805 (68%) had a CD4 test at some point
after enrollment], of which 6875 (50%) were ART eligible. Of
the eligible patients, 2886 (42%) initiated ART #90 days of
their first CD4 test [3635 (53%) initiated ART at some point].
Patient flows stratified by testing service type (VCT vs.
PMTCT) are displayed in Figure 1. VCT patient retention
dropped by 3% (to N = 16,232) between testing and enrollment, by an additional 34% (to N = 10,773) between enrollment and CD4 test, and of those who were eligible for ART,
an additional 54% (to N = 2565) between CD4 testing and
ART initiation. By contrast, PMTCT patient retention dropped by 7% (to N = 5657) between testing and enrollment, by
an additional 48% (to N = 2935) between enrollment and CD4
test, and of those who were eligible for ART, an additional
75% (to N = 321) between CD4 testing and ART initiation.
The overall proportions of HIV-positive patients progressing
through the care and treatment cascade out of the total number
tested are presented in Figure S1 (see Supplemental Digital
Content, http://links.lww.com/QAI/A494).
Enrollment in ART Clinics (Outcome 1)
Measures of Patient Flow
With VCT and PMTCT combined, 21,889 patients
(96%) enrolled at an ART clinic #30 days after testing HIV
ART clinic enrollment was not significantly different
between patients referred from PMTCT (58%) and VCT
centers (68%) (RR = 0.84, 0.72 , RR , 1.02) (Table 3).
TABLE 2. Selected Characteristics of Patients Enrolled in Study Clinics, by HIV Testing Center
VCT
N (%)
Total
Age
Mean 6 SD
Sex
Female
Education, yrs
0–5
6–9
$10
Missing
Marital status
Single
Married
Widow/separated
Missing
First CD4 count (cells per mm3)
Median (IQR)
Missing (%)
First WHO stage recorded
I/II
III
IV
Missing
Clinic type
Integrated
Vertical
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16,649 (73.2)
33.3 6 10.1
PMTCT
N (%)
Total
N (%)
6088 (26.8)
22,737 (100)
25.1 6 5.6
31.1 6 9.8
9886 (59.4)
6088 (100)
15,974 (70.3)
7498
6123
2058
970
(45.0)
(36.8)
(12.4)
(5.8)
2840
2323
523
402
(46.7)
(38.2)
(8.6)
(6.6)
10,338
8446
2581
1372
(45.5)
(37.2)
(11.4)
(6.0)
4638
9483
1999
529
(27.9)
(57.0)
(12.0)
(3.2)
1306
4447
159
176
(21.5)
(73.1)
(2.6)
(2.9)
5944
13,930
2158
705
(26.1)
(61.3)
(9.5)
(3.1)
258 (122–457)
2380 (14.3)
389 (239–584)
4449 (73.1)
289 (143–492)
6829 (30.0)
5884
6107
586
4072
3335
510
17
2226
9219
6617
603
6298
(35.3)
(36.7)
(3.5)
(24.5)
9329 (56.0)
7320 (44.0)
(54.8)
(8.3)
(0.3)
(36.6)
4656 (76.5)
1432 (23.5)
(40.6)
(29.1)
(2.7)
(27.7)
13,985 (61.5)
8752 (38.5)
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Linkages From HIV Testing to Care
TABLE 3. Univariate Log-Binomial Analyses of HIV Care Linkage by HIV Testing Center
Univariate
Enroll in ART clinic #30 d of testing HIV positive
VCT
PMTCT
Undergo CD4 test #30 d of enrollment
VCT
PMTCT
Initiate ART in #90 d of first CD4 test (if eligible)
VCT
PMTCT
N (%)
RR (95% CI)
P
16,232 (68)*
5657 (58)†
Ref
0.84 (0.72 to 1.02)‡
0.08
10,773 (45)*
2935 (30)†
Ref
0.79 (0.66 to 0.94)§
0.01
2565 (11)*
321 (3)†
Ref
0.51 (0.41 to 0.64)†§
,0.001
*Percentages are out of total patients who tested HIV positive and matched HIV sites, for VCT this is 23,817.
†Percentages are out of total patients who tested HIV positive and matched HIV sites, for PMTCT this is 9823.
‡Clustered at HIV testing center level.
§Clustered at clinic level.
Overall Treatment Outcomes
CD4 Testing (Outcome 2)
Of the 2886 patients who initiated ART in #90 days,
attrition from ART care by 180 days for any reason (death,
LFTU, or transferring out of the care network) was 8.9%
[95% confidence interval (CI): 7.9 to 10.0]. Of the 8.9%
who left ART care, 6.1% was due to death or LTFU, and
2.8% was due to transferring to another clinic.
Patients tested in PMTCT centers were less likely to
have a CD4 test #30 days after clinic enrollment (30%)
compared with VCT centers (45%) when adjusting for age,
education level, and marital status [adjusted RR (aRR) 0.84,
0.70 , aRR , 1.00] (Table 4).
Initiation of ART (Outcome 3)
Treatment Outcomes Stratified by
Testing Service
Eligible patients tested in PMTCT centers were less
likely to initiate ART #90 days after their first CD4 test (3%)
compared with patients tested in VCT centers (11%) when
adjusting for age, education level, and marital status (aRR =
0.56, 0.44 , aRR , 0.71) (Table 4).
For the 2565 patients tested at VCT centers, 180-day
all-cause attrition from ART care was 9.6% (95% CI: 8.6 to
10.8) compared with 2.8% (95% CI: 1.5 to 5.3) for the 321
TABLE 4. Multivariate Log-Binomial Analyses of HIV Care Linkage by HIV Testing Center
Undergo CD4 Test £30 Days of Enrollment
Factor
HIV testing center
VCT
PMTCT
Education, yrs
0–5
6–9
$10+
Age, yrs
15–19
20–29
30–39
$40
Marital status
Single
Married
Widow/separated
Initiate ART £90 Days of First CD4 Test (If Eligible)
Adjusted RR*† (95% CI)
P
Adjusted RR*‡ (95% CI)
P
Ref
0.84 (0.70 to 1.00)
0.05
Ref
0.56 (0.44 to 0.71)
,0.001
Ref
1.04 (1.00 to 1.08)
1.08 (0.99 to 1.17)
0.03
0.05
Ref
1.09 (1.00 to 1.20)
1.29 (1.10 to 1.52)
0.05
0.02
Ref
1.12 (1.05 to 1.19)
1.19 (1.10 to 1.29)
1.25 (1.12 to 1.39)
,0.001
,0.001
,0.001
Ref
1.10 (0.88 to 1.38)
1.16 (0.92 to 1.47)
1.29 (1.01 to 1.66)
0.39
0.20
0.04
Ref
1.11 (0.80 to 1.54)
1.15 (0.85 to 1.57)
0.52
0.37
Ref
1.04 (0.94 to 1.16)
1.19 (1.05 to 1.34)
0.44
0.01
*Clustered at clinic level.
†From 21,222 patients eligible, excluding 491 with missing marital status, 1118 with missing educational status, and 163 missing both, a total of 19,450 were included.
‡From 6429 patients eligible, excluding 132 with missing marital status, 371 with missing educational status, and 39 missing both, a total of 5887 were included.
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patients tested at PMTCT centers. Of the 9.6% who left ART
care and were tested at VCT centers, 6.7% was due to death
or LTFU and 2.9% was due to transferring. Of the 2.8% who
left ART care and were tested at PMTCT centers, 0.31% was
due to death or LTFU and 2.5% was due to transferring.
Delayed Outcomes
The proportion of patients who successfully proceeded
onto the next step of treatment, but did so beyond the time
restrictions, was higher for all 3 outcomes among patients
tested at PMTCT centers compared with VCT centers (enroll
at ART clinic: 6.2% of PMTCT versus 1.9% of VCT; CD4
testing: 5.4% of PMTCT versus 4.9% of VCT; initiate ART:
12.0% of PMTCT versus 10.6% of VCT). The median time
between HIV test to enrollment and from enrollment to CD4
was the same between the groups (0 and 3 days, respectively),
but median time from CD4 to ART was 43 days for VCT
(interquartile range, 27–74) and 63 days for PMTCT (interquartile range, 38–106).
Gender
When restricted to VCT alone, the percentage of males
and females who had a CD4 test and initiated ART was nearly
identical (CD4: 68% of females versus 69% of males; ART:
51% of females versus 49% of males).
DISCUSSION
Our investigation of the relationship between type of
HIV testing center and retention in HIV care demonstrated
consistent and substantial drop-offs at each step in the HIV
care cascade among patients diagnosed at both VCT and
PMTCT centers. Patients diagnosed at PMTCT centers were
significantly less likely to have a CD4 test and initiate ART
compared with patients diagnosed at VCT centers. ART clinic
enrollment was also lower among women tested at PMTCT
centers, although this result was not statistically significant.
Pre-ART retention across sub-Saharan Africa (SSA) is
heterogeneous.4 Our findings are similar to other studies done
from SSA reporting rates of linkage from HIV testing to ART
clinic enrollment and CD4 testing.12,13,19 Studies from Uganda and South Africa have reported a higher proportion of
ART-eligible patients starting ART than we found in this
study.8,11,13 Yet, this study found higher ART initiation than
previous studies in Mozambique.4,5
Lower pre-ART retention among HIV-positive pregnant
women referred from PMTCT centers is a common finding in
other studies. The results of this study in 18 clinics is similar to
a previous analysis from 2 clinics in the same region, which
demonstrated that compared with those referred from VCT
centers, patients referred from PMTCT centers were less likely
to enroll at an ART clinic #30 days from HIV testing, were
similarly likely to have a CD4 test done #30 days after ART
clinic enrollment, and were less likely to initiate ART #90
days of their CD4 test.5 Another study in Mozambique found
that ART-eligible women (including pregnant women) had
lower odds of initiating ART compared with men.20 Two stud-
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ies in South Africa also found that pregnant women had higher
rates of LTFU after starting ART compared with non-pregnant
patients.11,21 However, this relationship has not been consistent
across settings. One study in South Africa found that women
tested for HIV at PMTCT centers were more likely to have
a CD4 and initiate ART if eligible compared with patients who
were tested at VCT centers.13
Differences in retention between VCT and PMTCT
patients are not surprising given the many factors that influence
LTFU. First, gender may influence successful referral and
movement through the HIV care system; although the
influence of gender on LTFU is not consistent in the
literature6–8,11,12,19–24 nor was gender associated with LTFU
among the VCT population in this study. Second, because
pregnant women are routinely screened for HIV during antenatal care, they are generally healthier than patients who seek
HIV testing at VCT centers. Previous research has found lower
CD4 count to be predictive of retention in care,6–8,11,20–22,25–27
and the women from PMTCT testing centers in this study had
a higher median CD4 count and lower WHO stage at enrollment compared with the VCT group. Furthermore, pregnant
women who discover their HIV status through routine screening as part of antenatal care may be less prepared for the
diagnosis than those who actively seek testing, which may
impact subsequent HIV care.14 This result is consistent with
other literature that has found self-referral to HIV testing to be
associated with lower rates of LTFU compared with providerinitiated HIV testing.12 Another potential interpretation is that
women, especially pregnant women, may be more vulnerable
to stigma associated with an HIV diagnosis, which could easily
lead to LTFU.14 Although previous research on stigma among
patients who initiated ART in central Mozambique saw no
difference in stigma, depression, or perceived social support
between genders,28 it may be that LTFU in the pre-ART phase
of care may be more susceptible to these influences.
HIV testing and health system factors may also
influence the higher pre-ART LTFU among women tested
at PMTCT centers, especially related to limitations in
counseling and referral within busy antenatal care centers.
In southern Mozambique, “cultural miscommunication” was
documented between the PMTCT staff and patients when it
came to breastfeeding and future childbearing, and this miscommunication was found to be a barrier to receiving
PMTCT centers.29 Other studies documented transportation
costs and antenatal care wait times as other reasons for LTFU
in cohorts of pregnant women.14,19,29
There are several limitations of this study. First, we were
unable to match over 8000 patients who tested HIV-positive at
testing sites but were not matched to HIV sites using ART
clinic records, and we had moderate amounts of (.8%) patient
exclusion. To be included in this study, a patient had to both
test and receive care within the catchment area of the 18
included HIV care clinics. Therefore, if a patient tested outside
the network but sought care inside the network or vice versa,
they were not included. We cannot infer any information on
whether these unmatched patients are different from those who
did match; nevertheless, the proportion of tested patients who
matched were similar comparing those tested at VCT (77%)
versus PMTCT (65%) (Fig. 1). Regarding patient exclusion,
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J Acquir Immune Defic Syndr Volume 66, Number 2, June 1, 2014
this could contribute to selection bias; yet, most of our exclusions were because patients were younger than 15 years,
mainly acting to restrict our generalizability and not expected
to bias our findings.
Second, because data from HIV testing services were
only available as aggregate monthly reports, our analysis
could not follow individuals referred from HIV testing centers
to ART clinics. As a result, we could not adjust for individual
characteristics in the enrollment analysis (outcome 1), and the
lack of individual-level data may have led to inclusion of
more individuals under 15 years of age in the group tested in
VCT than PMTCT (where the great majority of pregnant
women are over 15 years of age). Although this limitation is
notable, we expect that this would overestimate LTFU
between testing and HIV care center enrollment among those
tested in VCT compared with PMTCT, which would have
attenuated the observed difference between those tested in
PMTCT and VCT. Routine data systems may also contain
errors, and although most of the data used in this study came
from ART databases that have been previously validated,
HIV testing center data systems have not been validated for
completeness or accuracy.5,15–18
Another study limitation is the lack of information on
reasons for HIV care attrition. Attrition from HIV care can be
divided into 4 categories: death, transfer, LTFU, or delayed
ART while remaining in care. Based on the available death
and transfer data, the proportion of patients tested at VCT
who died or transferred to another clinic was 10-fold than that
of PMTCT, which fits the pattern of more advanced HIV
disease among patients seeking VCT centers.25–27,30 It is
likely that undocumented mortality and transfers, especially
among VCT-referred patients, led to outcome misclassification and attenuated risk estimates. We also have no available
information on reasons for delays in moving through the HIV
care system because a greater proportion of patients tested at
PMTCT centers completed the study outcomes beyond the
time restrictions compared with those tested at VCT centers.
A final limitation is that we were unable to include
other testing centers of interest, including community-based
testing and testing in clinical services (primarily tuberculosis services). Patients tested for HIV at community and
clinic-based testing likely have different health and wellness patterns, and different experiences with linkages to the
health system.
Despite these limitations, this study has a number of
strengths. First, using a novel approach, we were able to link
HIV testing and ART clinic data to estimate not only preART LTFU within the HIV care system but also drop-offs
between testing and care centers. We were also able to
include data from multiple HIV testing centers and ART
clinics to describe referral and care patterns within a complex
HIV care system environment. A further strength of this study
is the large sample of study patients from 18 heterogeneous
HIV care systems (including testing centers and care clinics)
covering a large geographic area, which provides more stable
estimates of the pre-ART LTFU experience.
Further studies are needed to better understand the
barriers to initiating and continuing HIV care among pregnant
women in Mozambique and other areas of SSA. It is difficult
Ó 2013 Lippincott Williams & Wilkins
Linkages From HIV Testing to Care
to ascertain reasons for differential retention among pregnant
women in different ART care systems without information on
reason for LTFU. Further assessment of operational and
community factors associated with the high and differential
pre-ART LTFU, and testing of approaches to ameliorate this
LTFU, is critically needed to improve retention as ART
centers continue to expand. Additionally, improvements in
retention in HIV care will require further strengthening of the
overall health care system to accommodate the larger
numbers of patients who are enrolled and maintained in
long-term HIV care.
ACKNOWLEDGMENTS
The authors would like to thank the Ministry of Health
and the Beira Operations Research Center (CIOB) for their
support in the collection and analysis of data reported here.
The authors would also like to thank the clinic staff and
patients for participating in this research.
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